Aquatic Hemiptera community structure in stormwater retention ponds: A watershed land cover approach

Abstract

Stormwater ponds are increasingly common aquatic habitats whose biotic communities are largely unexplored. As anthropogenic
development continues to alter the landscape, watershed land use is gaining recognition for its potential to predict species
compositions in aquatic systems. This study reports species composition of five aquatic hemipteran families (Notonectidae,
Corixidae, Belostomatidae, Nepidae, Pleidae) in 28 permanent, artificial stormwater ponds in watersheds with different land
covers and associated contaminant input. We hypothesized that land cover variables would be significant drivers of aquatic
hemipteran community structure in ponds, and that ponds with a high percentage of agricultural and lawn cover in the watershed
would be characterized by the absence of species intolerant of the chemical, physical, and ultimately biotic changes associated
with these watersheds. Non-metric multi-dimensional scaling (NMS) was used to identify dominant gradients of species composition
and environmental variables. Pond morphology variables, watershed lawn, watershed agriculture, and predatory fish abundance
were each found to have statistically significant correlations with hemipteran community structure. The abundance of Notonecta undulata, the species responsible for creating the largest (ranked) distance in species structure among ponds, was positively correlated
with shallow, fishless ponds and independent of land use variables. The abundances of four species of corixids were negatively
correlated with watershed agriculture, and hemipteran richness was positively correlated with watershed lawn and negatively
correlated with pond surface area. Heirarchical cluster analysis revealed non-random hemipteran species assemblages in which
congeneric corixid species tended to co-occur, contradicting traditional niche theory. Since artificial stormwater ponds are
chemically different from natural-pond habitat and rapidly increasing in number, knowledge of which insect species are capable
of thriving in this environment and their relationship to land use in the watershed is of both environmental and evolutionary
interest.

Full text

PRIMARY RESEARCH PAPER
Aquatic Hemiptera community structure in stormwater
retention ponds: a watershed land cover approach
Sarah J. Foltz ÆStanley I. Dodson
Received: 26 June 2008 / Revised: 1 October 2008 / Accepted: 6 October 2008 / Published online: 11 November 2008
ÓSpringer Science+Business Media B.V. 2008
Abstract Stormwater ponds are increasingly com-
mon aquatic habitats whose biotic communities are
largely unexplored. As anthropogenic development
continues to alter the landscape, watershed land use is
gaining recognition for its potential to predict species
compositions in aquatic systems. This study reports
species composition of five aquatic hemipteran fam-
ilies (Notonectidae, Corixidae, Belostomatidae, Nepi-
dae, Pleidae) in 28 permanent, artificial stormwater
ponds in watersheds with different land covers and
associated contaminant input. We hypothesized that
land cover variables would be significant drivers of
aquatic hemipteran community structure in ponds, and
that ponds with a high percentage of agricultural and
lawn cover in the watershed would be characterized by
the absence of species intolerant of the chemical,
physical, and ultimately biotic changes associated with
these watersheds. Non-metric multi-dimensional scal-
ing (NMS) was used to identify dominant gradients of
species composition and environmental variables.
Pond morphology variables, watershed lawn,
watershed agriculture, and predatory fish abundance
were each found to have statistically significant
correlations with hemipteran community structure.
The abundance of Notonecta undulata, the species
responsible for creating the largest (ranked) distance in
species structure among ponds, was positively corre-
lated with shallow, fishless ponds and independent of
land use variables. The abundances of four species of
corixids were negatively correlated with watershed
agriculture, and hemipteran richness was positively
correlated with watershed lawn and negatively corre-
lated with pond surface area. Heirarchical cluster
analysis revealed non-random hemipteran species
assemblages in which congeneric corixid species
tended to co-occur, contradicting traditional niche
theory. Since artificial stormwater ponds are chemi-
cally different from natural-pond habitat and rapidly
increasing in number, knowledge of which insect
species are capable of thriving in this environment and
their relationship to land use in the watershed is of both
environmental and evolutionary interest.
Keywords Notonectidae Corixidae Lawn 
Agriculture Land use Anthropogenic change
Introduction
Suburban development in the United States is growing
at a conservative rate of 906 thousand hectares a year
(USDA, 2000), approximately 23% of which is
devoted to monoculture lawn (Robbins & Birkenholtz,
Handling editor: D. Dudgeon
S. J. Foltz S. I. Dodson (&)
Zoology Department, University of Wisconsin, Madison,
430 Lincoln Drive, Madison, WI 53706, USA
e-mail: sidodson@wisc.edu; sidodson@facstaff.wisc.edu
S. J. Foltz
e-mail: sarah@xerces.org
123
Hydrobiologia (2009) 621:49–62
DOI 10.1007/s10750-008-9631-6

2003), with the remaining land largely covered by
impervious surfaces. Since impervious surfaces
release storm water more quickly than undeveloped
land, retention ponds are designed to collect this run-
off and prevent its direct discharge into streams and
lakes (England, 2001). While virtually every water
body in the United States contains anthropogenic
chemicals (Gilliom et al., 2006), stormwater ponds
situated immediately in the drainage system of high
impact land cover (such as commercial agriculture and
chemically treated lawn) are incredibly vulnerable to
ground and surface water pollutants, including high
nutrient loads and chemicals intended specifically to
prevent, repel, or kill organisms (EPA, 2008). Widely
used organophosphate insecticides, for example, bind
to neurotransmitter enzymes and disrupt nervous
impulses, leading to death or altered behavior in
insects. Likewise, the herbicide 2,4-Dselectively
interferes with broad leaf plant growth, and is known
to kill several aquatic insects (PAN Pesticides Data-
base, 2007).
Since chemical input into water catchment basins
varies with land usage in the watershed (Tong & Chen,
2002), watershed land use may serve as a potential
predictor of aquatic communities (Hoffman & Dod-
son, 2005; Dodson, 2008). Studies have shown that
biotic response variables are strongly impacted by
both agricultural (Allan et al., 1997; Karaouzas &
Gritzalis, 2006) and residential watershed land cover
(Dodson, 2008; Lussier et al., 2008), both of which are
often associated with relatively homogeneous assem-
blages of species capable of tolerating high levels of
chemical and physical disturbance (Delong & Brus-
ven, 1998; Leisnham et al., 2007). While watershed
agriculture has a history of examination in landscape-
scale studies of stream communities (Allan, 2004), the
impact of agriculture on pond systems is less under-
stood. Additionally, the increasing sales and
application of insecticides, herbicides, fungicides,
and fertilizers in lawn care maintenance (Robbins &
Sharp, 2003) necessitates broadening our environmen-
tal focus on agricultural to include the high-input
suburban lawn (Robbins et al., 2001; Robbins &
Birkenholtz, 2003).
While studies have focused on the performance of
retention ponds and their ability to protect streams and
lakes (Hancock & Popkin, 2005), few studies have
examined the community structure patterns occurring
in the stormwater ponds themselves (Gingrich et al.,
2006). We chose to focus on fully aquatic hemipterans
because they are widespread insects capable of
colonizing nearly all types of aquatic habitats, and
are often one of the first successional stages in newly
created water bodies, such as artificial ponds (Papacek,
2001). Both herbivorous (most Corixidae) and carniv-
orous (Notonectidae, Belostomatidae, Nepidae,
Pleidae), these bugs have considerable influence on
aquatic food webs, feeding on zooplankton, insects,
and small vertebrates, and serving as prey for large
insects and fish (e.g., Murdoch et al., 1984; Hickley
et al., 1994; Blaustein, 1998; Gilbert & Burns, 1999;
Hampton et al., 2000). Additionally, the economic
importance of at least three of these families as
biological control agents of disease-carrying mosqui-
tos is well established (Nam et al., 2000; Saha et al.,
2007, reviewed in Papacek, 2001). Notonectids, in
particular, have been shown to prey preferentially on
mosquito larvae, drive mosquitoes to local extinction
(Murdoch et al., 1984), and even deter oviposition
behavior in gravid mosquitoes, including Anopheles
gambiae, the primary vector of human malaria (Blau-
stein et al., 2005; Munga et al., 2006).
The goal of this project was to study landscape-scale
aquatic hemipteran community composition in a
multispecies system whose organisms are confronted
with numerous anthropogenic inputs in some of the
habitats. Chemical contaminants have profound lethal
and sublethal effects in aquatic systems, altering
community structure and function (Rohr & Crumrine,
2005) via the physiological and behavioral processes
of aquatic organisms within (Fleeger et al., 2003). In
natural systems, however, limited pesticide application
data and increasingly unmanageable numbers of
manufactured chemical products, break-down prod-
ucts, and undisclosed inert ingredients often hinder the
study of direct chemical-to-community relationships.
Given the elusive identity of the contaminants whose
combined effects are under scrutiny, we proposed an
investigation in which community structure was
studied in relation to high-impact land cover associated
with elevated levels of pesticide use, such as commer-
cial agriculture and chemically treated lawns. In
addition to watershed land cover, six other environ-
mental variables recognized in the literature as drivers
of aquatic hemipteran assemblages were measured:
fish abundance, macrophyte abundance, conductivity,
pond age, water depth, and surface area (e.g., Briers &
Warren, 2000; Svensson et al., 2000). Multivariate
50 Hydrobiologia (2009) 621:49–62
123

techniques were used to test the relationships between
environmental variables and hemipteran community
structure, and to examine the co-occurrence tendencies
of the species in this system. We hypothesized that land
cover variables would be significant drivers of aquatic
hemipteran community structure in ponds, and that
ponds with a high percentage of agricultural and lawn
cover in the watershed would be characterized by the
absence of certain species intolerant of the chemical,
physical, and ultimately biotic changes associated with
these watersheds. Since artificial stormwater ponds are
chemically different from natural-pond habitat and
rapidly increasing in number, knowledge of which
insect species are capable of thriving in this environ-
ment and their relationship to land use in the watershed
is of both environmental and evolutionary interest.
Methods
Twenty-eight permanent artificial stormwater reten-
tion ponds in Dane County, Wisconsin, were selected
for this study (Dodson, 2008). Ponds differ in water-
shed land cover, age, surface area, depth, and vege-
tation structure, but are relatively similar in landscape
position, conductivity, and substrate composition
(Dodson, 2008). Each pond is the sole body of water
in its watershed basin. The extent of each watershed
was determined by walking each site and using USGS
topographic maps and orthographs (30-cm resolution)
from http://accessdane.co.dane.wi.us/. Watershed
land cover was categorized as lawn, agriculture (corn/
soy), impervious surfaces, and low-impact (meadow/
woods), and the area of each category was quantified
from high-resolution orthographic photos, available
through Wisconsin Department of Natural Resources
Webview (http://dnrmaps.wisconsin.gov/imf/imf.jsp?
site=webview). Webview was also used to determine
the surface area of the ponds. Water depth was mea-
sured or estimated at the deepest point in each pond in
June. The sites varied in age from two to 22 years old,
as determined from city records, land owner inter-
views, or by personal observation (Dodson, 2008).
Water temperature, specific conductance, total dis-
solved solids (TDS), salinity, and dissolved oxygen
percent were measured at the time of each insect
sampling. Specific conductance was the only water
chemistry variable included in the multivariate
analyses.
Hemiptera sampling
Each pond was sampled for aquatic insects between
June 10th and 20th, and again between September 8th
and 16th, 2007. Relative abundance sampling was
conducted by pulling a 4.35 m-by-1.15 m beach seine
(1 mm-by-1.5 mm mesh) through a 13 m stretch of the
pond, spanning both littoral and limnetic zones.
‘‘Target’’ sampling was also conducted by running a
D-frame aquatic net through several sites in the pond
chosen to maximize the differences in vegetation or
substrate type. This method also helped ensure the
collection of very small or fast bugs. Seine and ‘‘target’’
samples were preserved separately in 70% ethanol for
identification. Adult hemipterans were identified to
species, and the sex and age class of notonectids and
corixids were determined. Species-level identification
was possible for notonectid instars III–V, but all other
hemipteran instars were identified to genus (noto-
nectids, nepids) or family (corixids), unless species
designation could be inferred by repeated single-
species collections (e.g., only one species of Belos-
toma,Neoplea, and Buenoa were collected in this study
regardless of season, therefore the nymphs were also
assigned to the pertinent species).
Biotic community variables
Each pond was seined for predatory fish in June and
September by pulling a beach seine (described above)
through three 13-m stretches of each pond. Fish
abundance was combined across seasons and catego-
rized between one and five, based on natural breaking
points in the distribution of abundance values. Actual
abundance values ranged from 0 to 349. Vegetation
surveys were also conducted at this time, and the
percentage cover occupied by submerged macrophytes
was estimated by walking, wading, and raking the
pond perimeter. Dominant plant species were collected
and identified. For comparability with Dodson (2008),
emergent macrophytes, floating macrophytes, and
algae were not included in percentage cover values.
Statistical analysis
Individuals collected in ‘‘target’’ samples were not
included in the analyses unless they represented a
species not collected by the seine sample of that pond
in either season. This was most commonly the case
Hydrobiologia (2009) 621:49–62 51
123

for the very smallest bugs (Corisella tarsalis Fieber,
Trichocorixa species, and Neoplea striola Fieber),
although all of these species were capable of
collection by the seine as well. Rare species (found
in less than three ponds) were omitted from multi-
variate analyses (McCune & Grace, 2002), but
included in the instability/seasonality analysis. Spe-
cies instability (I) was calculated for each species as
the number of times it changed its presence–absence
status in the ponds between June and September:
I¼X
28
i¼0jpSept
ipJune
ijwhere pseason
i2f0;1g
¼absence;presence
The seasonality (S) of these changes was calcu-
lated to show the net change in presence–absence
between the sample dates:
S¼X
28
i¼0
pSept
ipJune
iwhere pseason
i2f0;1g
¼absence, presence
Apart from these analyses, the June and September
data were summed (for abundance data) or unionized
(for presence–absence data).
Resemblance matrices were created for the ponds
using species abundance data (Bray–Curtis distance
measure) and normalized environmental data (Euclid-
ean distance measure) using PC-ORD (McCune and
Mefford 2006). The relationships between species
composition and environmental variables were exam-
ined using the Mantel test, which tests the hypothesis
that species and environmental similarity matrices are
not related in multivariate structure using the Pearson
correlation method and Mantel’s asymptotic approx-
imation for test-statistic evaluation (McCune & Grace,
2002). The Best analysis (BIOENV algorithm, in
PRIMER) was used to select the environmental
variables ’’best explaining’’ species community pat-
tern by maximizing a rank correlation between their
respective resemblance matrices. Community struc-
ture (species by ponds) was analyzed with Non-metric
multi-dimensional scaling (NMS) from PCORD5
(McCune & Mefford 2006). NMS avoids the assump-
tion of linear relationships among variables (species
abundances) and is recommended for data with lots of
zeros (McCune & Grace 2002). In our case, the data
matrix was 61% zeros, which represented species that
were absent from a particular pond. Correlation of
species data with the NMS axes indicated the species
most important in determining community structure.
Correlation of environmental variables with the NMS
axes indicated which variables were candidates for
drivers of community structure. The environmental
variables included watershed landcovers, pond age,
depth, surface area, conductivity, fish abundance, and
macrophyte abundance. For visualization, the joint
biplot generated by the ordination was rotated to align
the first axis with the species causing the largest (Bray–
Curtis) differences between ponds (Notonecta undu-
lata Say). Three ponds were extreme outliers in the
ordination biplot, probably because they were the only
ponds that contained only one species. Therefore, they
were subsequently omitted from further multivariate
analyses in order to more clearly see the relationship
between species and environmental variables in the
other ponds.
Heirarchical cluster analysis of species assem-
blages based on presence–absence data was
conducted using the Bray–Curtis distance measure
and the group average linkage method (McCune &
Grace, 2002) in PRIMER. The SIMPROF permutation
procedure was used to test for significance (5% level)
of the resulting clades (Clarke & Gorley, 2006). The
use of presence–absence data in this analysis served to
uncover relationships involving species with low
abundance but high frequencies of occurrence.
Results
Twenty-six of the 28 artificial retention ponds were
found to support aquatic hemipterans. In total, 9989
specimens were identified to species, representing 26
species from five families (Notonectidae, Corixidae,
Belostomatidae, Nepidae, Pleidae) (Table 1). Corixi-
dae was the most species-rich family; 17 corixid
species were identified, one of which, Corisella
inscripta Uhler, had not been previously documented
in Wisconsin (Hilsenhoff, 1995; Chordas, et al.,
2002). Although some species were very common
and abundant, others were relatively rare, occurring
in low numbers and at few sites (Table 1). Notonecta
undulata (Notonectidae) was by far the most common
and abundant species, occurring in 23 ponds, and
accounting for 39% of the total species abundance.
Sex ratios of notonectid species and Hesperocorixa
52 Hydrobiologia (2009) 621:49–62
123

corixid species were generally not different from 1:1,
while the sex ratios of Sigara and Trichocorixa
corixid species were generally female-biased
(Table 1). Percentage of adults generally increased
from June to September (Table 1).
Aquatic hemipteran richness ranged from one to
16 species in the occupied ponds (Table 2); seven
was both the mean and the mode species richness
value. Corixid richness ranged from one to 12 species
(Table 2), with two species the mode and 4.6 species
the mean. The 26 ponds also showed variation in
morphology, biotic variables, and percent composi-
tion of each watershed land cover category (Table 2).
Sixteen of the 28 ponds supported fish, with a total of
five species (all predatory) collected. The fathead
minnow (Pimephales promelas, a pioneer species
highly tolerant of a wide range of environmental
conditions (Scott & Crossman, 1973)) was most
common, occurring in 11 ponds. Green sunfish
(Lepomis cyanellus), bluegills (Lepomis macrochi-
rus), and goldfish (Carassius auratus) occurred in six,
four, and three ponds, respectively, while largemouth
bass (Micropterus salmoides) were found in just one
pond. Potamogeton species were the most common
dominant submerged macrophytes in this system,
although a few of the well-vegetated ponds had
relatively homogeneous populations of Eurasian
milfoil (Myriophyllum spicatum).
Table 1 The 25 aquatic hemipteran (Nepomorpha) species encountered in the 28 retention ponds over two sample periods
Family Species Occurrence Abundance % Fem % Ad June % Ad Sep
Belostomatidae Belostoma flumineum 16 77 8.33 39.29
Corixidae Corisella inscripta 5 792 55.7
Corixidae Corisella tarsalis 5 28 74.2
Corixidae Hesperocorixa atopodonta 4 6 50.0
Corixidae Hesperocorixa laevigata 5 49 52.0
Corixidae Hesperocorixa obliqua 17 1130 55.4
Corixidae Hesperocorixa scabricula 8 96 51.0
Corixidae Hesperocorixa vulgaris 10 62 63.9
Corixidae Sigara alternata 21 668 83.2
Corixidae Sigara decorata 5 179 68.7
Corixidae Sigara defecta 7 15 86.7
Corixidae Sigara grossolineata 2 3 0.0
Corixidae Sigara solensis 1 1 0.0
Corixidae Trichocorixa borealis 3 12 77.8
Corixidae Trichocorixa calva 6 27 64.1
Corixidae Trichocorixa kanza 6 55 59.7
Corixidae Trichocorixa sexcincta 6 30 38.7
Nepidae Ranatra sp. (fusca,kirkaldyi,nigra) 8 13 20.0 50.0
Notonectidae Buenoa margaritaceae 13 2143 58.4 33.3 74.7
Notonectidae Notonecta insulata 13 481 49.3 32.8 98.8
Notonectidae Notonecta lunata 3 3 0.0 100.0
Notonectidae Notonecta undulata 23 4078 50.8 47.3 76.5
Pleidae Neoplea striola 7 40 84.8 0.0
Occurrence indicates the number of ponds that the species was found in, while abundance indicates the total number of individuals
that were sampled from those ponds. The sex ratio (% Fem) indicates the percentage of adults that were female; the age ratio (% Ad)
indicates the percentage of the species that were adults, separated by sample date. Blank cells are shown for sex or age ratios not
acquired. Age ratios were not acquired for corixid species (blank cells) due to the inability to identify the instars of this taxon
(Hilsenhoff 1995). The age ratio of Corixidae (16 species combined) was 52% adults in June and 79% in September. Due to their low
numbers and similarity in habitat and resource use, Ranatra species were combined in our analyses; R. fusca was the most common of
the three species. Hemipteran species with occurrence values less than three were not included in the NMS ordination or cluster
analysis
Hydrobiologia (2009) 621:49–62 53
123

Strong seasonality was expressed by the notonect-
ids Buenoa margaritacea Torre-Bueno and Notonecta
insulata Kirby, both of which expressed consistently
positive (B. margaritacea) or consistently negative
changes (N. insulata) in presence/absence status in the
ponds between June and September (Fig. 1). Buenoa
margaritacea was found in six ponds in June (total
abundance =29) and in six additional ponds in
September (total abundance =474). In contrast,
N. insulata was found in 13 ponds in June (total
abundance =407), and no longer found in six of those
ponds in September, when its total abundance dropped
to 79. The highest instability values were found for the
corixid species Sigara alternata Say (10 changes) and
Hesperocorixa vulgaris Hungerford (nine changes),
the changes of which were only weakly seasonal
(Fig. 1). Belostoma flumineum Say and Hesperocorixa
laevigata Uhler were also relatively unstable,
Table 2 Environmental variables and richness values (Hemiptera and Corixidae) for each pond
Pond Latitude Longitude Area
(m
2
)
Depth
(m)
Cond
(lhos/cm)
Age
(years)
%
Imperv
%
Lawn
%
Ag
%
Mead/
Wd
%
Macro
Fish
(Ab.C.)
Het
SR
Cor
SR
A1 43.0400 89.2454 3441 3.0 0.333 9 6.3 12.5 26.4 51.4 100 4 0 0
A2 43.0166 89.3010 809 2.0 0.264 3 37.2 43.1 0.0 16.8 30 4 16 11
A3 43.0709 89.2597 405 1.0 0.129 2 13.3 79.3 0.0 4.4 80 2 12 6
A4 43.0916 89.2663 4452 2.0 0.163 7 48.4 41.1 0.0 8.9 5 5 2 1
A5 43.0749 89.2798 3642 2.2 0.196 14 24.3 24.8 28.8 21.6 0 2 12 8
A7 43.0603 89.4992 8903 2.0 0.318 13 66.9 26.5 0.0 5.4 0 5 7 4
A8 43.0396 89.5241 4047 2.0 0.152 6 34.8 9.4 28.7 27.1 1 5 1 0
A9 43.1151 89.4921 809 1.0 0.434 3 72.2 20.6 0.0 6.2 40 1 7 5
A10 43.1087 89.4956 1619 1.5 0.299 12 54.2 15.6 0.0 26.6 30 1 7 2
A11 43.0764 89.2058 405 1.5 0.142 2 84.0 11.8 0.0 0.0 50 3 7 5
A12 43.0766 89.2070 4047 1.5 0.192 4 34.0 20.7 8.7 36.7 10 4 0 0
A13 43.1506 89.2884 5261 2.0 0.180 6 27.2 20.6 0.0 50.7 20 5 12 8
A14 43.0197 89.2996 1214 1.0 0.211 2 6.3 45.2 0.0 47.6 0 5 15 12
A15 43.0722 89.7648 93 1.0 0.146 2 4.0 4.7 3.4 87.2 2 1 7 2
A16 43.1437 89.2755 405 1.5 0.207 2 74.4 23.2 0.0 0.0 50 1 9 5
A17 43.2281 89.7222 186 0.7 0.339 2 0.0 0.0 0.0 100.0 80 1 4 1
A18 43.2301 89.7206 287 1.5 0.251 2 0.0 0.0 0.0 100.0 5 1 9 4
A19 43.0723 89.1320 174 1.0 0.215 12 0.7 0.0 0.0 97.8 60 1 8 2
A20 43.0706 89.8131 182 2.0 0.597 19 0.0 0.0 1.6 97.5 80 1 5 2
A21 43.0261 89.2842 10522 2.0 0.281 8 34.0 64.2 0.0 0.9 0 3 1 1
A22 43.0266 89.2843 1619 2.0 0.162 4 40.1 48.2 0.0 10.9 10 3 9 6
A23 43.0843 89.2676 279 0.7 0.352 2 13.2 23.3 0.0 63.6 0 1 6 4
A25 43.1602 89.2710 40000 3.0 0.374 6 8.1 1.6 71.8 16.9 15 5 2 0
A27 43.1656 89.4273 405 1.5 0.084 6 37.8 22.8 33.8 5.3 30 1 5 2
A28 43.0374 89.4289 445 1.0 0.297 22 52.0 40.0 0.0 8.0 45 1 9 5
A29 43.0371 89.4331 3035 2.0 0.254 22 32.5 22.3 0.0 44.2 10 1 10 7
A30 42.9987 89.5273 2023 2.0 0.089 20 3.6 0.0 0.0 93.5 0 5 8 4
A32 43.0877 89.2568 5261 2.0 0.143 8 47.2 24.0 18.1 9.7 0 3 1 1
The conductivity values and percent submerged macrophyte values reported here were measured during the June sample period.
Richness values reflect species occurrences over both the June and September sample periods. Ponds with zero (A1, A12) or one (A8,
A21, A32) aquatic hemipteran species were excluded from multivariate analyses. Cond =conductivity, Imperv =impervious land
cover, Lawn =lawn land cover, Ag =agricultural land cover, Mead/Wd =least impact meadow and wooded land cover,
Macro =submerged macrophytes, Fish (Ab.C.) =Fish abundance category (1 =no fish, see methods), Het SR =Aquatic
hemipteran species richness, Cor SR =Corixidae species richness. The land cover percentages do not appear to sum to 100 because
the percent water in the watershed is not shown
54 Hydrobiologia (2009) 621:49–62
123

non-seasonal species (Fig. 1). Species that were fairly
consistent in their occurrence across seasons (detected
by the combination of low instability and low season-
ality values) included both very rare (e.g., Sigara
solensis Hungerford) and very common species (e.g.,
N. undulata) (Table 1, Fig. 1).
Non-metric multi-dimensional scaling (NMS)
revealed patterns of hemipteran assemblages (Fig. 2),
and agreement was found between rank dissimilarities
in the Bray–Curtis matrix and distances among sites in
ordination space (stress =6.20%). The correlation
between environment and species variables in multi-
dimensional space was validated by the Mantel test
(R=0.363, P=0.003). Water depth and watershed
agriculture were identified as the environmental
variables contributing the most to this relationship
(Best test, see methods). The ordination joint biplot
enabled differences in community structure between
ponds to be evaluated in terms of environment and
species variables. All species and environmental
variables portrayed as vectors on the joint biplot
are significant at the 0.05 level (Table 3). Since
N. undulata was responsible for creating the largest
(ranked) distance in species structure between ponds,
it was chosen as the species variable to align with
axis 1 (Fig. 2). The abundance of this species was
negatively correlated water depth and fish abundance,
and independent of watershed land cover. The
9
131335
22
335
6
1
122
5
38
4
310
4
2
-7
-6
-5
-4
-3
-2
-1
0
1
2
3
4
5
6
7
Notonecta insulata
Sigara defecta
Trichocorixa calva
Trichocorixa borealis
Trichocorixa sexcincta
Sigara grossolineata
Belostoma flumineum
Sigara decorata
Ranatra fusca
Ranatra kirkaldyi
Notonecta undulata
Sigara solensis
Corisella tarsalis
Trichocorixa kanza
Ranatra nigra
Neoplea striola
Hesperocorixa laevigata
Corisella inscripta
Hesperocorixa obliqua
Hesperocorixa scabricula
Notonecta lunata
Sigara alternata
Hesperocorixa atopodonta
Hesperocorixa vulgaris
Buenoa margaritacea
<-------
June
---------- Seasonality ------------ Sept. ------->
Fig. 1 Occurrence instability and seasonality of 25 aquatic
hemipteran species sampled from 28 ponds in June and
September. Species whose seasonality values were highly
positive tended to be absent in June but present in September,
particularly when the seasonality value was equal to the
instability value (e.g., B. margaritacea). Species with highly
negative seasonality values tended to decline in September,
again, particularly when the seasonality value (absolute value)
was equal to the instability value (e.g., N. insulata). Species
with seasonality values close to zero were highly consistent in
their presence/absence status in ponds, if their instability value
was also low. Low seasonality values coupled with high
instability values indicates that the species had several
countering (non-directional) occurrence changes (e.g., B.
flumineum)
Hydrobiologia (2009) 621:49–62 55
123

abundance of Hesperocorixa obliqua Hungerford, a
large corixid species, also followed this same pattern.
Axis 2 was largely driven by four smaller corixid
species (Corisella tarsalis Fieber, Corisella inscripta
Uhler, Trichocorixa calva Say, and Sigara decorata
Abbott) each expressing a negative association with
agricultural land cover in the watershed (Fig. 2).
Aquatic hemipteran richness, although not strongly
correlated with either axis individually, was posi-
tively correlated with watershed lawn, and negatively
correlated with pond surface area. Agriculture and
lawn were the only land cover categories significantly
correlated with the relationship between ponds based
on species composition. Low-impact land cover
(woods, meadow), impervious surface, pond age,
macrophyte abundance, and conductivity had no
relationship to species variables in multidimensional
space.
Cluster analysis using Bray–Curtis similarity
revealed the non-random co-occurrence of certain
Fig. 2 The NMS biplot of environmental and species corre-
lates overlayed on the pond-by-species ordination. Ponds were
separated based on Bray–Curtis distance in species abun-
dances. Notonecta undulata was the species variable most
correlated with one of the axes (i.e., did the best job separating
the ponds based on ranked distance), therefore the graph was
rotated to align this species with Axis 1. Each species and
environmental vector displayed in the graph is significantly
correlated with one of the axes at the 0.05 level (Pearson and
Kendall test). Vector lengths indicate the strength of the
correlations with the axes. Of the environmental variables
tested, pond morphology variables, watershed land cover
percentages, and fish abundance were all correlated with
species structure. Of the land cover variables, only the high-
impact categories (percent agriculture and percent lawn) were
significantly correlated with species structure. In addition to N.
undulata, five corixid species (C. tarsalis,C. inscripta,S.
decorata,T. calva, and H. obliqua), and hemipteran richness
have significant relationships with the projected community
structure. Ag =Agriculture, WaterDep =Water Depth, H
Rich =Hemipteran Richness, H.obl =Hesperocorixa obli-
qua, N.und =Notonecta undulata, S.dec =Sigara decorata,
T.cal =Trichocorixa calva, C.ins =Corisella inscripta,
C.tar =Corisella tarsalis
Table 3 Significant correlations (Pearson and Kendall test) of
environmental and species variables with the NMS ordination
axes (Critical rvalue for significance at the 0.05
level =0.404)
Axis 1 Axis 2
rr
2
rr
2
Pond area -0.585 0.343 0.569 0.324
Water depth -0.429 0.184 0.068 0.005
Lawn 0.355 0.126 -0.368 0.135
Agriculture -0.286 0.082 0.519 0.269
Fish abund -0.46 0.211 -0.177 0.031
C. inscripta 0.197 0.039 -0.523 0.274
C. tarsalis 0.38 0.144 -0.632 0.4
H. obliqua 0.432 0.187 0.073 0.005
S. decorata 0.107 0.011 -0.433 0.187
T. calva 0.23 0.053 -0.436 0.19
N. undulata 0.759 0.576 0.139 0.019
Hem richness 0.609 0.371 -0.586 0.343
56 Hydrobiologia (2009) 621:49–62
123

hemipteran species in these ponds (Fig. 3). Notonecta
undulata,S. alternata, and H. obliqua have 89%
similarity in the ponds in which they occur. This
clade is significant at the 0.05 level (SIMPROF test).
Interestingly, the three other significant clades with
high similarity values consisted of species-pairs
belonging to the same corixid genus (Fig. 3).
Discussion
Despite their vulnerability to chemical and physical
disturbance, permanent stormwater retention ponds
are an important habitat for many species of aquatic
bugs (Table 1). The tendency of B. margaritacea to
increase in abundance and occurrence between early
summer and early fall (Fig. 1) is consistent with
reports in the literature. This species differs from the
other notonectids in this system in both its over-
wintering strategy (as eggs, rather than adults)
(Hilsenhoff, 1995), and in the lengthy gestation
period of the eggs. Buenoa species generally have a
gestation period of approximately 42–77 days (Bare,
1926), while Notonecta eggs develop in as little as 3–
14 days (Clark & Hersh, 1939). The tendency of
N. insulata to decrease in abundance and occurrence
between early summer and early fall may be due to
this species’ intolerance of high water temperatures
(Streams, 1987b). Warm, shallow pond-conditions
(more common at the end of summer) are probably
inhospitable to this species (Streams, 1987b). Several
species were found to be highly consistent in their
occurrence across seasons (low instability and sea-
sonality), usually denoting their very rare (e.g., S.
solensis) or ubiquitous (e.g., N. undulata) pattern of
distribution (Fig. 1, Table 1). The high instability of
S. alternata and H. vulgaris and, to a lesser extent, B.
flumineum and Hesperocorixa laevigata, indicate that
these species frequently migrate in and out of ponds,
or else maintain their presence in a pond but are
difficult to capture and detect. Based on these
findings, one sample event is not enough to assess
the presence of all hemipterans in a small aquatic
habitat, and repeated sampling regimes are especially
critical for detection of the seasonal and instable
species reported here (Fig. 1).
Non-metric multi-dimensional scaling (NMS)
revealed the importance of both local and landscape
scale variables in governing hemipteran species
structure in ponds. This result is consistent with a
recent study of Heteroptera species assemblages in
streams, in which local and regional variables
Fig. 3 Habitat co-occurrence tendencies of 21 aquatic hemi-
pteran taxa sampled from 28 ponds. Cluster analysis of species
assemblages was based on presence/absence data, and per-
formed using the Bray–Curtis distance measure. The hierarchy
of the dendrogram was determined by group average fusion.
Circles indicate significant clades (0.05 level, SIMPROF test)
with high similarity values ([75%). Clades 1, 2, and 3 each
consist of corixid species belonging to the same genus. Clade 4
consists of three extremely common species with relatively
high abundance values (Table 1). Taxa are abbreviated as:
F(amily): G(enus) s(pecies); species names can be found in
Table 1
Hydrobiologia (2009) 621:49–62 57
123

accounted for the most variation in community
structure, and assemblages at the regional scale were
mainly divided into those found in agricultural and
forested landscapes (Karaouzas & Gritzalis, 2006).
The abundant and ubiquitous distribution of N. undu-
lata and H. obliqua in stormwater retention ponds
indicate their tolerance to a wide array of species
compositions and anthropogenic land use in the
watershed. Although N. undulata is a strong flier with
high dispersal potential and the ability to colonize
almost any freshwater environment (Hilsenhoff, 1984;
Papacek, 2001; Chordas et al., 2005), the tendency of
this species to colonize shallow, fishless ponds (Fig. 2,
Bennett & Streams, 1986) may be due to direct
avoidance of fish predators (e.g., sunfish, Crowder &
Cooper, 1982) or to indirect selection of smaller,
shallower ponds (e.g., Svensson et al., 2000) in which
fish are less likely to prosper. Streams (1987a) noted a
major division in the Notonecta species colonizing
habitat with and without insectivorous fish, and
proposed that the foraging strategy of N. undulata
(active search) when compared to N. lunata Hunger-
ford and other congenerics (sit and wait), may explain
this species’ poor adaption to fish (Streams, 1987a). In
controlled fishless environments, however, the forag-
ing efficiency (prey capture/predator, three types of
prey) of N. undulata far exceeds that of N. lunata and
N. insulata (Streams, 1987a), the two less common and
abundant Notonecta species in our study (Table 1).
Additionally, unlike N. insulata,N. undulata displays
tolerance to high water temperatures which often
occur in shallow ponds (Streams, 1987b). Artificial
stormwater ponds tend to be shallow, sparsely vege-
tated, and prone to high levels of contamination
(Dodson, 2008). Tolerance to such factors may give N.
undulata and other opportunistic species a competitive
advantage in anthropogenically influenced habitat, and
their potential to displace less tolerant species in the
current landscape should be examined.
Axis 2 of the NMS ordination biplot was largely
driven by four smaller corixid species (C. tarsalis,
C. inscripta,T. calva, and S. decorata) each expressing
a negative association with agricultural land cover in
the watershed (Fig. 2). This relationship suggests an
anthropogenic source of pollution affecting agricul-
tural ponds, and also indicates that these species are
more sensitive to the aquatic environment imposed by
watershed agriculture than that by lawn or impervious
surface. Specific impacts of agricultural pollution on
corixids have been documented; for example, the
dietary exposure of Trichocorixa reticulata Say to
subsurface agricultural drainage can result in the
accumulation of selenium in the insect’s body
(Thomas et al., 1999). Tissue residues of the aquatic
herbicide dichlobenil have also been found to accu-
mulate rapidly in exposed Sigara dorsalis Leach and
Corixa punctata Illiger, inhibiting elytral pigmenta-
tion in both nymphs and newly developed adults
(Tooby & Macey, 1977).
Given the negative impact of watershed lawn on
the richness and abundance of other aquatic taxa
(e.g., zooplankton and amphibians) (Dodson, 2008),
the positive relationship between aquatic hemipteran
richness and watershed lawn was unexpected
(Fig. 2). If lawn is indeed the main driver of richness
increases in this system, then the potential shift in
hemipteran composition from sensitive to insensitive
taxa (e.g., Lussier et al., 2008) deserves attention.
Neither impervious surface nor conductivity was
related to community structure, suggesting inconsis-
tent or complex effects of these variables on pond
habitat and community. Pond age and submerged
macrophyte abundance, both of which have been
shown to increase richness in other insect taxa (e.g.,
dragonflies, Kadoya et al., 2004) also had no
relationship to species variables in multidimensional
space (Fig. 2). Although it is clear that aquatic
vegetation is a major food and resource for many of
these bug species (Hilsenhoff, 1984), submerged
macrophytes also impose structural complexity which
can have negative effects on predatory species by
reducing predation rates and providing a refuge for
prey (Cook & Streams, 1984). The lack of relation-
ship between macrophytes and hemipteran
community structure is consistent with the finding
that species richness is not negatively affected by
herbicide-intensive lawns in the watershed (Fig. 2).
Herbicides kill both terrestrial and aquatic plants, but
aquatic hemipterans (particularly N. undulata, the
main driver of community structure in this system) do
not appear to be affected by the loss of plants. While
the limited influence of vegetation on Notonecta
species has been reported (Bennett & Streams, 1986;
Briers & Warren, 2000), the apparent lack of
relationship between corixid abundance and sub-
merged macrophytes is somewhat surprising, since
these herbivores use aquatic vegetation to meet
dietary needs (Hilsenhoff, 1984). A more sensitive
58 Hydrobiologia (2009) 621:49–62
123

(species level) measure of plant and algal resources
would likely enable clearer assessment of their
influence on corixids and other herbivorous taxa. In
this system, Potamogeton species were the most
common dominant macrophytes, although a few of
the well-vegetated ponds had relatively homogeneous
populations of Eurasian milfoil (Myriophyllum
spicatum), which was not found to support aquatic
hemipterans (e.g., Pond A1, Table 1, 100%
M. spicatum cover).
Heirarchical cluster analysis identified non-ran-
dom distribution patterns of certain species of
hemipterans. Notonecta undulata,S. alternata, and
H. obliqua were the three species with the highest
similarities (89%) in pond occurrence (Fig. 3).
Although two of these species share the positive
association with smaller, shallower ponds (Fig. 2), all
three were among the most common and abundant
species in this system (Table 1), indicating their
tolerance to a wide array of species compositions and
anthropogenic land use in the watershed. Interest-
ingly, H. obliqua has recently been identified as a
species of greatest conservation need (Wisconsin
Department of Natural Resources, 2005), probably
due to reports by Hilsenhoff (e.g., 1970) noting the
rarity of this species compared with H. vulgaris.
Natural ponds and wetlands, such as those sampled
by Hilsenhoff, were once the major habitat for
aquatic bugs. However, in the past 150 years, more
than half of Wisconsin’s original 10 million acres of
wetlands and ponds have been filled in or drained
(Dodson & Lillie, 2001), most of this loss occurring
in Southern Wisconsin. In the current landscape,
natural lentic habitat has largely been replaced by
artificial ponds, many of which are the result of 2001
state legislation (NR151) which dictates the creation
of retention ponds for storm water management
practices (Dodson, 2008). The opposite-of-expected
relative abundances of H. obliqua and H. vulgaris
encountered in this study (Table 1) may reveal a
species shift due to anthropogenic habitat change.
Cluster analysis also highlighted the co-occurrence
tendencies of several corixid congenerics (Fig. 3).
Traditionally, the tendency of closely-related species
to co-occur is assessed in terms of similar habitat
requirements (which would drive species together)
and competition for limited resources (which would
drive them apart) (e.g., Briers & Warren, 1999). Body
size is an important factor in the competitive potential
between aquatic hemipterans, and species of similar
body sizes should have increased competition relative
to species of different body sizes (Svensson et al.,
2000). Indeed, the distribution patterns of corixids in
this system appear to be best explained by genus-
level differences in body size; however, body size
similarity serves to unite, rather than separate, closely
related species (Fig. 3). Species of Trichocorixa are
the smallest corixids in Wisconsin (*3 mm), those
of Hesperocorixa are the largest (*11 mm) and
those of Corisella are intermediate (*7.5 mm)
(Hungerford, 1948). Given those size disparities,
our results contradict predictions of traditional niche
theory in which similar-sized species do not co-occur
(Hutchinson, 1962). Rather, it appears that the
distribution pattern of these corixids is strongly
influenced by non-competitive size-related interac-
tions with the pond habitat or community, such as
size-selective predation by waterfowl, fish, and/or
aquatic insects (Dodson et al., 1994).
In summary, results of this study suggest that both
agriculture and lawn in the watershed alter habitat
quality in such a way as to have consistent impacts on
hemipteran community structure. Chemical inputs,
which vary with land usage in the watershed (Tong &
Chen, 2002), are the most obvious mechanism for the
relationships between land cover and species reported
here, since pesticides, like predators, elicit density
and behaviorally mediated changes in select species
(Fleeger et al., 2003; Relyea & Hoverman, 2006),
which can, in turn, have profound impacts at the
population and community levels (Dill et al., 2003,
Rohr & Crumrine, 2005, Rothley & Dutton, 2006,
reviewed in Schmitz et al., 2004 and Werner &
Peacor, 2003).
Community structure is traditionally evaluated in
terms of random dispersal followed by non-random
competition, predation, and resource-related mortal-
ity. The chemical sensitivity of insects, however,
suggests the importance of non-random dispersal in
systems of heterogeneous chemical habitat. Oviposi-
tion habitat selectivity (OHS) provides an interesting,
largely overlooked, mechanism for community assem-
bly in which species composition is largely limited by
the frequency and success of surrounding populations’
selective dispersal events via the use of highly specific
visual, tactile, and/or chemical cues (e.g., A
˚bjornsson
et al., 2002; Blaustein et al., 2004,2005; Binckley &
Resetarits, 2005). As increasing research demonstrates
Hydrobiologia (2009) 621:49–62 59
123

the importance of OHS in structuring aquatic insect
populations, communities, and metacommunity
assemblages (Resetarits, 2005; Encalada & Peckarsky,
2006), questions arise as to the maintenance of this
highly evolved, often chemically mediated behavior in
anthropogenically altered chemical environments.
Anthropogenic contaminants are a ubiquitous (Gilliom
et al., 2006), but relatively recent environmental
phenomena and it is unclear whether they are general
enough, or have persisted long enough, to be perceived
by the odor and taste receptors of ovipositing/migrat-
ing aquatic insects (receptors reviewed in Hallam
et al., 2006; olfaction in Rutzlerm & Zwiebel, 2005).
Comparison between the field data, presented here,
and experimental monitoring of hemipteran migration
into water from different watersheds would help reveal
if the species present/absent in high impact ponds are
able to perceive and select/avoid water chemistry
associated with watershed land use, or if observed
community differences in ponds with different
watershed land cover are better explained by non-
contaminant-related selection criteria and/or variation
in post-colonization survival and success. Despite
their undesirable presence in the environment, aquatic
contaminants associated with watershed land cover
may provide useful insight into the sensory percep-
tions, migration behaviors, and community structure
patterns in aquatic insect assemblages. Artificial
stormwater ponds are readily accessible, highly rep-
licated, and understudied aquatic environments in
which to observe these unique toxicological effects.
The need for this line of investigation is growing as the
abundance of these ponds within the current landscape
begins to alter what limnologists think of as aquatic
habitat, and arguably, what aquatic invertebrates call
home.
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